Orchid Extinction Over the Last 150 Years in the Czech Republic

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Article Orchid Extinction over the Last 150 Years in the Czech Republic

Zuzana Štípková 1,2,* and Pavel Kindlmann 1,2

1 Global Change Research Institute, Academy of Sciences of the Czech Republic, Bˇelidla986/4a, 60300 Brno, Czech Republic; [email protected] 2 Institute for Environmental Studies, Faculty of Science, Charles University, Benátská 2, 12801 Prague, Czech Republic * Correspondence: [email protected]; Tel.: +420-7367-31008

Abstract: Understanding temporal changes in the distribution and abundance of various species is one of the key goals of conservation biology. During recent decades, the abundance and distribution of many species of plants and animals have declined dramatically, mainly because of habitat loss and fragmentation. The purpose of this study is to analyze the rate of extinction of orchids at various sites in different 20-year time intervals over the last 150 years, determined according to changes in society. Using the dataset of the orchid records of the Nature Conservation Agency of the Czech Republic, we determined the disappearance rate of orchids from sites using a grid of 1 × 1 km. We found that the vast majority of orchids disappeared from many of their historical localities in all time intervals analyzed. The number of sites suitable for Czech orchids declined by 8–92%, depending on the species. The most threatened orchid species in the Czech Republic are Spiranthes spiralis, Anacamptis palustris, Epipogium aphyllum and Goodyera repens. This all seems to be closely related with changes in agricultural practices in the open as well as in forest habitats. Preserving suitable orchid habitats seems to be the key for keeping Czech orchid flora alive. Keywords: conservation; number of sites; critically endangered orchids; threatened Citation: Štípková, Z.; Kindlmann, P. Orchid Extinction over the Last 150 Years in the Czech Republic. Diversity 2021, 13, 78. https://doi.org/ 10.3390/d13020078 1. Introduction One of the most important issues of modern conservation biology is to understand Academic Editors: Mark Brundrett temporal changes in the distribution and abundance of various species [1]. During recent and Mario A. Pagnotta decades, the human impact on natural resources and habitats has caused a dramatically large extinction rate and a decline in the number of sites suitable for many plants and Received: 15 January 2021 animals [2–7], with habitat loss and fragmentation being the most important factors [2,3]. Accepted: 9 February 2021 Mankind has had a very marked effect on Europe, especially its rapid industrial devel- Published: 13 February 2021 opment in recent centuries, which has resulted in a highly fragmented and degraded landscape [8]. The current land cover in Europe is mainly a result of farming and demo- Publisher’s Note: MDPI stays neutral graphic trends over recent decades [9]. In general, urbanization, changes in land use and with regard to jurisdictional claims in the intensification of agriculture are the most important factors that have resulted in habitat published maps and institutional affil- destruction in many parts of Europe [5,6,10–12]. iations. In the past, there were important changes in the use of land in the Czech Republic (Czechoslovakia, until the splitting of the country in 1993), which differed from those that occurred in Western Europe because of the differences in the political regimes in Central and Western Europe [13,14]. Before 1948, fields and meadows were traditionally managed [15], Copyright: © 2021 by the authors. which involved mowing and grazing, low intensity agriculture of small fields and low Licensee MDPI, Basel, Switzerland. application of fertilizers [14]. After 1948, small fields were combined into huge fields [16] This article is an open access article and subsidies for fertilizers were provided, which resulted in the amount of chemicals distributed under the terms and in the soil increasing rapidly [14]. After the change of regime in 1989, the subsidies for conditions of the Creative Commons fertilizers stopped, which resulted in a great decline in the use of fertilizers [17]. Attribution (CC BY) license (https:// In this study, we concentrate on orchids, because orchids are considered to be one of the creativecommons.org/licenses/by/ most threatened groups of species worldwide [18–20]. With approximately 28,500 species [21], 4.0/).

Diversity 2021, 13, 78. https://doi.org/10.3390/d13020078 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 78 2 of 15

Orchidaceae is one of the most diverse and widespread families of flowering plant [18]. Unfortunately, most species of orchids are threatened in the wild [22] and are disappearing from their natural habitats worldwide [7,22–24]. In Europe, the main reasons for this dramatic decline are habitat loss, eutrophication and fragmentation [12,23,25–28]. Their typical low pollination success and low levels of fruit set, as well as environmental heterogeneity, are also linked to their rarity [29–31]. Because of the activities of professionals and amateurs, orchids are well recorded and studied in many countries in Europe [32]. The availability of detailed records collected over long periods of time provides opportunities for comparative analyses of the declines of a species over time [23]. Identification of environmental factors and species traits that are correlated with the decline in the orchid’s distribution could result in improvements in the management of valuable habitats [23]. However, despite the increasing number of studies dealing with orchid distribution in different parts of the world e.g., [33–38], there is scarce information available on orchid conservation and the drivers of their extinction [31,39]. An important category of orchids that requires special conservation measures is those orchids classified in the most threatened category according either to the IUCN guidelines or other national classifications e.g., [8,40,41]. These lists of species provide essential information on trends in the loss of biodiversity [42–44]. Red List assessments often differ among countries [45] and are therefore more appropriate for local conditions than IUCN Red List categories and criteria [46], which were built to be as general as possible. However, some general patterns at the landscape level might be found using national Red List data [43,47]. Therefore, we use the latest Czech Red List [48] here. The aim of this study was to analyze the trends in the changes in the number of sites of rare species of orchids (those classified as “critically endangered” and “extinct” based on the national Red Lists) [40,41,48]. We attempted to put the available data into context with shifts in agricultural practices. We asked the following questions: From what percentage of historically known sites did orchids disappear over the time period covered by our database (about 150 years)? Is there any difference in the number of sites from which orchids disappeared before, during and after the communist period in the Czech Republic? Which species of orchids in the Czech Republic are most in danger of becoming extinct, based on the percentage of historical sites still occupied?

2. Materials and Methods 2.1. Study Site The Czech Republic is in central Europe and its ﬂora is very well studied. Its average altitude is 450 m above sea level, a calculation based on the 30-sec altitude layer [49] and performed in ArcMap 10.1 [50]. The country is covered mainly by highlands of moderate altitude, whereas higher mountains occur at the borders with other countries (mainly in the north and south). The climate of the Czech Republic is typically temperate, with cold, cloudy winters and hot summers. However, there are some regional and local differences due to the relief that forms the complex topography in this area [51]. Because the Czech Republic is a relatively small country in terms of latitude range, temperature and precipitation are mostly affected by local heterogeneity and altitude [52].

2.2. The Database The dataset of orchid records we used is based on that of the Nature Conservation Agency of the Czech Republic, which is not freely accessible. The records cover a period of about 150 years and include all known literature and reports from people on the records of orchids, the identities of which are subsequently checked by specialists. The database includes more than 115,000 individual records. Each site is characterized by its GPS coordinates. Because of the high number of records and the extremely long timespan covered, the cross-checking procedure for dupli- cate records was not consistently conducted, especially in the older data. This means that Diversity 2021, 13, 78 3 of 15

in many cases, the same site may be called different names and the GPS coordinates may differ for the same sites in different records in the database. We resolved this problem by using ArcMap 10.1 [50] to create a grid of 1 × 1 km squares. For each square, we then considered any recording with its GPS coordinates falling within this square as the same site. This is reasonable, as typical orchid sites cover several thousand square meters, and small adjacent sites are likely to be sub-sites of a larger site, or, in other words, an orchid meta-population. For each of the sites (squares in our grid where an orchid population was recorded), we determined the latest year when orchids were still present at the site. If the year was 1990 or later, the site was considered still occupied (except in the case of two species mentioned in Section 3.1, which are commonly considered extinct in the Czech Republic, despite being found during 1990–2020). If the last record of an extant population at a site was prior to 1990, this date was considered to be the date of extinction of the orchid population at this site. It is unlikely that this resulted in a bias in our calculations. First, in case of rare species of orchids, which is exclusively the case considered here, the Nature Conservation Agency of the Czech Republic meticulously re-checked all of the sites where these orchids were likely to survive. Second, if the date of the last record was prior to 1990, then the population might of course have survived for several additional years after this observation. However, as the dates of extinction are categorized into 20-year intervals (Table1), it is most likely that the actual date of extinction is in the same 20-year period as the date of the last record.

Table 1. Explanation of the selected time periods.

Time Period Explanation Before 1900 Very old data from the 19th century 1901–1918 Prior to the end of the 1st World War and the founding of Czechoslovakia 1919–1938 During the existence of the “1st” Czechoslovak Republic 1939–1948 2nd World War and the period before the Communist Putsch in 1948 1949–1968 Czechoslovakia under the Communist regime, before the Prague Spring 1969–1989 The period after the Soviet invasion and before the Velvet Revolution 1990–2020 The period after the Velvet Revolution and the free market economy in Czechoslovakia

2.3. Nomenclature The classiﬁcation, nomenclature and Red List classiﬁcation (threat categories) of native taxa are based on Grulich [41,48] and Danihelka et al. [40]. The threat category of Himan- toglossum adriaticum was taken from the Botany webpage [53], as there is information that H. adriaticum is still present at one locality in the Czech Republic, despite Danihelka et al. [40] referring to it as an extinct taxon.

2.4. Data Analysis We categorized a total of 64 species of orchids into threat categories based on the Red List classiﬁcation for the Czech Republic [40,41,48]. For the purpose of this study, we analyzed only the 34 species that are in the extinct (A1) and critically endangered (C1) categories. We categorized the A1 and C1 species according to the number of sites recorded in the database: species extinct in 2020, species recorded at less than 20 sites, species recorded at 21–100 sites, species recorded at 101–300 sites, species recorded at 301–1400 sites, and the special case of the newly described species Epipactis. Within each of these categories, we ranked the species according to the percentage of sites at which they survived up to the present time, from the lowest to the highest. For each species, we calculated the number of sites at which extinction was recorded during the selected time periods (see Table1). Thus, we mainly considered the political events most likely to have affected agricultural practices as milestones, rather than what was recorded at a particular interval of time. Diversity 2021, 13, 78 4 of 15

We looked for patterns of when orchids disappeared from sites for the different species and attempted to associate them with changes in society and political regimes that resulted in severe changes in agricultural practices. The results we present in the ﬁgures for each interval are the number of sites for which the latest year of the orchid’s presence at the site was in that particular interval. These are referred to as “newly unoccupied sites”. The reason for this notation is that—as we described above—if a site was never recorded as occupied later than this interval, the orchid in question probably went extinct during this interval. The sites recorded as occupied in last interval are considered currently occupied.

3. Results and Discussion The total number of sites for each species that were included in our database (i.e., which were recorded over the last 150 years), together with the percentages of those that remained occupied up to the present time, is shown in Table2. In the following sub-sections, the results are individually analyzed for a selected group of orchids in each of the time intervals outlined in the Data Analysis section.

Table 2. The total number of sites and their proportion occupied at the last interval for each orchid species analyzed in the Czech Republic. Species in red are considered to be extinct (category A1 in the national Red Lists) in the Czech Republic in 2020 according to available literature [40,41,53,54].

Total Sites Total Sites Species Number of Occupied Species Number of Occupied Sites (%) Sites (%)

Anacamptis coriophora 210 Goodyera repens 231 15 Anacamptis morio 750 49 Gymnadenia densiﬂora 199 65 Anacamptis palustris 159 13 Gymnadenia odoratissima 15 47 Anacamptis pyramidalis 176 40 Hammarbya paludosa 42 36 Dactylorhiza bohemica 7 71 Herminium monorchis 120 Dactylorhiza curvifolia 6 17 Himantglossum adriaticum 24 25 Dactylorhiza incarnata 282 68 Limodorum abortivum 47 49 Dactylorhiza maculata 355 37 Liparis loeselii 87 53 Dactylorhiza traunsteineri 28 46 Malaxis monophyllos 124 45 Epipactis futakii 1 100 Neotinea tridentata 40 30 Epipactis leptochila 49 90 Neotinea ustulata 885 28 Epipactis moravica 11 100 Neottia cordata 350 34 Epipactis nordeniorum 10 100 Ophrys apifera 72 92 Epipactis pontica 25 88 Ophrys holoserica 120 41 Epipactis pseudopurpurata 12 100 Ophrys insectifera 89 42 Epipactis talosii 23 96 Orchis mascula 1483 89 Epipogium aphyllum 201 16 Spiranthes spiralis 237 6

3.1. Extinct Species Figure1 shows the results for the four species that are now considered to be extinct. Although for two species (Dactylorhiza curvifolia and Gymnadenia odoratissima) some sites existed during the beginning of the last period (1990–2020), the recent agreement [40,41,48] is that all of them are now extinct. It is clear that this was dramatic in the case of Anacamptis coriophora, as it disappeared from 15 sites between the First and Second World War. The last two sites that remained after the Second World War were recorded as newly unoccupied before the Velvet revolution in 1989. The reasons for this are probably changes in the management of meadows and overall environmental pollution [54]. Anacamptis coriophora is one of the most threatened orchids in several European countries—it is extinct in Flanders Diversity 2021, 13, x FOR PEER REVIEW 5 of 15

Figure 1 shows the results for the four species that are now considered to be extinct. Although for two species (Dactylorhiza curvifolia and Gymnadenia odoratissima) some sites existed during the beginning of the last period (1990–2020), the recent agreement [40,41,48] is that all of them are now extinct. It is clear that this was dramatic in the case of Anacamptis coriophora, as it disappeared from 15 sites between the First and Second World War. The last two sites that remained after the Second World War were recorded as Diversity 2021, 13, 78 newly unoccupied before the Velvet revolution in 1989. The reasons for this are5 probably of 15 changes in the management of meadows and overall environmental pollution [54]. Anacamptis coriophora is one of the most threatened orchids in several European countries—it is extinct in Flanders and the Netherlands [55] and is one of the most and the Netherlands [55] and is one of the most quickly declining species in France, Belgium quicklyand Luxembourg declining species [56]. in France, Belgium and Luxembourg [56].

FigureFigure 1. The 1. numberThe number of sites of in sites particular in particular intervals intervals for the for four the four species species that that are arenow now considered considered to tobe be extinct extinct in in the the Czech Republic.Czech Republic.

DactylorhizaDactylorhiza curvifolia curvifolia andand HerminiumHerminium monorchismonorchiswere were only only recorded recorded at a at few a sitesfew sites in in the Czech Republic (6 and 12, respectively) and disappeared from these sites at almost the the Czech Republic (6 and 12, respectively) and disappeared from these sites at almost same rate over the period of this study. Kull et al. [12] identified H. monorchis as one of thethe same most rate threatened over the speciesperiod in of Europe. this study.Herminium Kull et monorchis al. [12] identifiedwent extinct H. aftermonorchis the Velvet as one of theRevolution most threatened in 1989, species mainly becausein Europe. of the Herminium changes in monorchis agriculture went and extinct the afforestation after the ofVelvet Revolutionmeadows in and 1989, pastures mainly [53]. because The situation of the with changesD. curvifolia in agricultureis a bit complicated. and the afforestation According of meadowsto the records and inpastures the database, [53]. itThe was presentsituation even with after 1990.D. curvifolia However, is literature a bit datescomplicated. the Accordinglast confirmed to the locality records to the in 1930s the [database,53] or 1953 it [54 was]. These present inconsistencies even after could 1990. be caused However, literatureby incorrect dates identification the last confirmed in the field. locality Moreover, to some the historical1930s [53] records or of1953 this species[54]. These inconsistenciesfrom 1930s are could classified be caused as the later by describedincorrectDactylorhiza identification bohemica in the[54 field.] or D. Moreover, traunsteineri some in 1970s [53]. historical records of this species from 1930s are classified as the later described The case of Gymnadenia odoratissima is very interesting. This species was also only Dactylorhizarecorded at bohemica 15 sites during [54] or the D. 20th traunsteineri century, and in these1970s sites [53]. were steadily recorded as newly unoccupiedThe case fromof Gymnadenia the beginning odoratissima of the Second is Worldvery interesting. War, half (seven) This of species which were was newly also only recordedunoccupied at 15 after sites 1990. during The lastthe confirmed 20th century, locality, and in WhitetheseCarpathians, sites were wassteadily destroyed recorded by as newlyintensive unoccupied cattle grazing. from the However, beginning suitable of habitatsthe Second are still World present War, in Whitehalf (seven) Carpathians, of which wereand newly there isunoccupied still a small after chance 1990. of recordingThe last thisconfirmed species therelocality, in the in futureWhite [54Carpathians,]. The wasregion destroyed of distribution by intensive of this cattle species grazing. is restricted Howeve to Europe.r, suitable It is classified habitats asare a potentiallystill present in Whiteendangered Carpathians, species and in Slovakia there is [53still] and a small is rare chance in Sweden of recording [57]. this species there in the future3.2. [54]. Species The with region 1 to 20 of Sites distribution of this species is restricted to Europe. It is classified as a potentiallyFigure2 shows endangered the results species for thein Slov fiveakia species [53] that and were is rare recorded in Sweden historically [57]. at 1 to 20 sites. For the three species for which more than 40% of the incidence of newly unoccupied sites was recorded, it seems that the number of newly unoccupied sites before the Second World War compared with those after the Second World War (i.e., before or after 1939) is larger for Neotinea tridentata and Hammarbya paludosa, and smaller for

Himantoglossum adriaticum. None of these differences, however, were statistically signiﬁcant Diversity 2021, 13, x FOR PEER REVIEW 6 of 15

3.2. Species with 1 to 20 Sites Figure 2 shows the results for the five species that were recorded historically at 1 to 20 sites. For the three species for which more than 40% of the incidence of newly unoccupied sites was recorded, it seems that the number of newly unoccupied sites before the Second World War compared with those after the Second World War (i.e., Diversity 2021, 13, 78 6 of 15 before or after 1939) is larger for Neotinea tridentata and Hammarbya paludosa, and smaller for Himantoglossum adriaticum. None of these differences, however, were statistically significant (t-test, p > 0.05). In Europe, H. adriaticum is found from the British Isles and t p H. adriaticum France to central European( -test, > Russia, 0.05). In extendin Europe, g to northernis found Scandinavia from the Britishand northernmost Isles and France to central European Russia, extending to northern Scandinavia and northernmost Italy; elsewhere, Italy; elsewhere, it is very rare [58]. Now, only three sites are extant in the Czech it is very rare [58]. Now, only three sites are extant in the Czech Republic, with the other Republic, with the otheroccurrences occurrences having vanished,having vanished, apparently apparently due to eutrophication due to eutrophication followed by succession [58]. followed by successionBódis [58]. et al. Bódis [59] conclude et al. [59] that conclude the decline that in the dry decline grasslands in dry due grasslands to the abandonment of due to the abandonmenttraditional of traditional land-use practices land-use (mowing practices or grazing) (mowing is the or mostgrazing) serious is the threat most to H. adriaticum serious threat to H. inadriaticum Hungary. in Hungary.

Figure 2. The blue columns are the number of sites that were occupied by orchids for the last time during the given interval Figure 2. The blue columns are the number of sites that were occupied by orchids for the last time during the given and then no longer occupied for the ﬁve species that were found historically at 1 to 20 sites. The green bar indicates the interval and then no longer occupied for the five species that were found historically at 1 to 20 sites. The green bar number of sites observed as extant in the last interval, which we consider as extant currently. indicates the number of sites observed as extant in the last interval, which we consider as extant currently. For Dactylorhiza traunsteineri (46% of sites still occupied) there is no difference between For Dactylorhizathe traunsteineri pre-1939 and post-1939(46% of periodssites still (t-test, occupied)p > 0.05). there The results is nofor differenceDactylorhiza bohemica between the pre-1939must and be post-1939 treated with periods caution, (t-test, because p > this 0.05). is a newlyThe results described for speciesDactylorhiza probably derived bohemica must be treatedfrom D. with traunsteineri caution, [because60]. It is this considered is a newly endemic described to the species CzechRepublic, probably and the two derived from D. traunsteinerirecently known [60]. populationsIt is considered are found endemic within to a protectedthe Czech area Republic, that seems and not the to be currently threatened [61]. two recently known populations are found within a protected area that seems not to be currently threatened3.3. [61]. Species with 21 to 100 Sites There are 10 species that occur historically at 21 to 100 sites (Figure3). For three of these (Anacamptis palustris, Epipogium aphyllum, Goodyera repens), less than 20% of the sites are currently occupied. For Anacamptis palustris, the critical period was 1969–1989, when

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3.3. Species with 21 to 100 Sites Diversity 2021, 13, 78 There are 10 species that occur historically at 21 to 100 sites (Figure 3). For7 three of 15 of these (Anacamptis palustris, Epipogium aphyllum, Goodyera repens), less than 20% of the sites are currently occupied. For Anacamptis palustris, the critical period was 1969–1989, when itit disappeared disappeared fromfrom 5151 (one(one third) third) of of its its historical historical sites. sites. For For the the latter latter two two species, species, the the numbernumber of sites newly unoccupiedunoccupied before before 1939 1939 was was signiﬁcantly significantly greater greater than than those those newly newly unoccupiedunoccupied after 19391939 ((t-test,t-test, p p= = 0.02 0.02 for forG. G. repens repensand andp =p 0.002= 0.002 for forE. aphyllumE. aphyllum). ).

Figure 3. The blue columnsFigure are the 3. Thenumber blue of columns sites that are thewere number occupied of sites by thatorchids were for occupied the last by time orchids during for the the last given time interval and then no longerduring occupied the givenfor the interval 10 species and then that no were longer found occupied historically for the 10 at species 21 to that100 weresites. found The green historically bar indicates the number of sitesat occupied 21 to 100 in sites. the Thelast greeninterval, bar indicateswhich we the consider number to of be sites the occupied current interval. in the last interval, which we consider to be the current interval.

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This disparity may be due to both being small forest species and, therefore, easily overlooked by orchid hunters willing to go to forests to look for orchids, which at that time was not a priority. It was found that G. repens is highly specific to its habitat [54,62] and sensitive to soil nutrients, which makes this species a good indicator of forest succession [62]. This might be the reason for its decline in the Czech Republic, where its decrease lies in excessive forest management [54]. In Ukraine, anthropogenic factors eliminate its populations [63]. The results for E. aphyllum should be treated with caution because the appearance of this species above ground is very irregular, and it can remain dormant for several years [64]. However, this species is considered extremely rare in Hungary [65] and one of the rarest orchids in Britain, facing an extinction risk in the near future [66]. A further six species in this group disappeared from 40–53% of their sites. Visual inspection of Figure3 indicates that there might be some increase in the number of sites newly unoccupied in the more recent time intervals, at least for some species. A t-test (p > 0.05) reveals that if the year 1939 is taken as a breakpoint, there are no differences between the pre-1939 and post-1939 time intervals. In contrast, however, if the year 1948 (the onset of communism in the Czech Republic) is considered as a breakpoint, the number of newly unoccupied species in the post-1948 time intervals is significantly (or almost significantly) larger than those pre-1948 for Ophrys insectifera (t-test, p = 0.003) and Malaxis monophyllos (t-test, p = 0.06—close to significance). For Liparis loeselii, the t-test is not significant, but the p value (p = 0.08) is relatively small, although it exceeds 0.05. It would be interesting to test whether the period of communism really affected the disappearance of O. insectifera, M. monophyllos and maybe even L. loeselii. This goes far beyond the scope of this paper. Possible candidates explaining this potential phenomenon might be the loss of suitable habitats for O. insectifera (and partly also for M. monophyllos) as it mainly occurs in pastures and grasslands, which were often changed into fields in the past. A possible explanation for the loss of many localities of L. loeselii might be hidden in changes in the water regime in the swamps, moors and bogs which this species favors. Similarly, Kaplan et al. [58] stated that the majority of populations disappeared in the late 19th century or during the first half of the 20th century due to direct habitat destruction (including drainage and conversion to arable land) and as a result of mowing abandonment and eutrophication followed by succession. The situation has improved recently [67], but the seed bank in the soil might not be sufficient for re-establishment in its previous localities. The last species in this group, Ophrys apifera, is a real puzzle. Despite a relatively large number of historical sites (72), it only disappeared from six during the 150 years covered by this study. Why O. apifera has survived so well is unknown. One possible explanation might be that this species is highly valued and so its numbers and localities are closely monitored and its habitats protected. This species was also mentioned as a new orchid for Sweden [68].

3.4. Species with 101 to 300 Sites Out of the six species, for which 101–300 sites were recorded in the database (Figure4 ), Spiranthes spiralis, with the extremely low survival rate of its historical sites (only 6/%), is outstanding. Almost half of these sites (105 out of 237) went extinct even before 1900. Previous studies from Europe [23,55,69–71] suggest that the huge decline in S. spiralis populations is linked to the loss of its natural habitats, mainly because of agricultural intensiﬁcation and the cessation of traditional management practices. We assume that these changes also play a role in the case of the population loss of S. spiralis in the Czech Republic. Diversity 2021, 13, x FORDiversity PEER 2021REVIEW, 13, 78 9 of 15 9 of 15

Figure 4. The numberFigure of sites 4. The that number were ofoccupied sites that by were orchids occupied for the by orchidslast time for during the last the time given during interval the given and interval then were and thenno were no longer occupied for longerthe six occupied species forthat the were six speciesfound thathistorically were found at 101 historically to 300 sites. at 101 The to 300 green sites. bar The indicates green bar the indicates number the of number of sites observed as extantsites in observed the last as interv extantal, in which the last we interval, consider which as weextant consider currently. as extant currently. Among other species, in Dactylorhiza maculata, the number of newly unoccupied Among othersites species, after 1948 in seems Dactylorhiza to be visually maculata larger, the than number that before of 1948,newly but unoccupied the difference is not sites after 1948 seemsstatistically to be significant visually larger (t-test, thpan= 0.05).that before No trends 1948, are but observable the difference for the is other not species, statistically significanteither (t -test,(t-test,p = p 0.05). = 0.05). No trends are observable for the other species, either (t-test, p = 0.05).The site survival rate of four out of the six species contained in this group (S. spiralis, The site survivalNeotinea rate ustulata of four, Neottia out of cordata the ,sixD. species maculata )contained is smaller thanin this 40%, group while (S. the spiralis survival, rate of Neotinea ustulatathe, Neottia remaining cordata two, (D.Gymnadenia maculata) densiflora is smaller, Dactylorhiza than 40%, incarnata while) the is larger survival than rate 60%. We can of the remainingonly two speculate (Gymnadenia as to whatdensiflora is causing, Dactylorhiza these differences. incarnata) is larger than 60%. We can only speculate3.5. as Species to what with is More causing Than 300these Sites differences. There are only two species with more than 300 sites among the endangered and 3.5. Species with criticallyMore Than endangered 300 Sites orchids: Anacamptis morio and Orchis mascula (Figure5). Both of them There are onlyshow two a similar species pattern: with a large more survival than rate300 ofsites their among sites (about the halfendangered for A. morio andand almost critically endangered90% for orchids:O. mascula Anacamptis). There are morio no significant and Orchis trends mascula between (Figure different 5). timeBoth intervals of in them show a similarthe past pattern: (t-test, ap large= 0.05). survival The recorded rate of hightheir survivalsites (about rate ofhalf these for twoA. morio species and over time almost 90% forin O. the mascula Czech Republic). There could are beno attributedsignificant to antrends increased between sampling different effort during time the last two decades. This is because the number of orchidologists (both experts and amateurs) intervals in the past (t-test, p = 0.05). The recorded high survival rate of these two species increased compared to that during previous periods, and both species are now well studied over time in thein thisCzech country Republic [25,28 ,could72]. be attributed to an increased sampling effort during the last two decades. This is because the number of orchidologists (both experts and amateurs) increased compared to that during previous periods, and both species are now well studied in this country [25,28,72].

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Figure 5. The number of sites that were occupied by orchids for the last time during the given Figure 5. The number of sites that were occupied by orchids for the last time during the given interval and then were no longer occupied for the two species that were found historically at more interval and then were no longer occupied for the two species that were found historically at more thanthan 300 300 sites. sites. The The green green bar bar indicates indicates the the number number of of sites sites observed observed as as extant extant in the last interval, whichwhich we we consider consider as as extant currently. 3.6. New Species of Epipactis 3.6. New Species of Epipactis Finally, Figure6 shows the situation for the newly described species of the genus EpipactisFinally,, other Figure than 6Epipactis shows ponticathe situationand Epipactis for the tallosii newly, which described were ﬁrst species recorded of the in thegenus Epipactisperiod 1919–1938, other than in Epipactis the database. pontica Because and Epipactis the recorded tallosii, history which ofwere these first species recorded is very in the periodshort, one1919–1938 cannot drawin the any database. conclusions Because from the these recorded data. history of these species is very short, one cannot draw any conclusions from these data.

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Figure 6. The blueFigure columns 6. The are blue the columns number are of the sites number that were of sites occupied that were by occupied orchids byfororchids the last for time the during last time the during given the given interval interval and thenand were then no werelonger no occupied longer occupied for the seven for the species seven of species the genus of the Epipactis genus .Epipactis The green. The bar green indicates bar indicates the number the number of sites of sites occupiedoccupied in the last in interval, the last interval,which we which consider we considerto be the tocurrent be the situation. current situation.

3.7. General Analysis3.7. General Analysis Figure 7 showsFigure the situation7 shows thefor situationspecies of for orchids species in of the orchids Czech in Republic the Czech with Republic less with less than than 50 sites occupied50 sites occupiedin the last in period, the last ranked period, in ranked order of in the order number of the of number occupied of occupied sites sites in the in the last periodlast (blue period bars). (blue The bars). orange The orangebars indicate bars indicate the percentage the percentage of their of original their original sites still sites still occupiedoccupied (the rate (the of rate decline of decline of the of number the number of their of theirsites siteshistorically). historically). The four The four encircled encircled speciesspecies occupy occupy less less than than 50 50 sitessites inin the the most most recent recent (last) (last) period period and, simultaneously, and, their simultaneously,present their present number numb of siteser isof lesssites than is less 20% than of that 20% of of all that their of sitesall their in the sites database. in Therefore, the database. Therefore,we conclude we that conclude these species that these need species urgent protection.need urgent These protection. species areTheseSpiranthes spiralis, species are SpiranthesAnacamptis spiralis palustris, Anacamptis, Epipogium palustris aphyllum, Epipogiumand Goodyera aphyllum repens .and The ﬁrstGoodyera two of these species repens. The firstoccur two in of open these habitats, species mainly occurmeadows in open andhabitats, pastures, mainly and meadows their decline and is caused by the pastures, and theircessation decline of traditionalis caused by management the cessation and of the traditional use of artiﬁcial management fertilizers. and Similar the results were use of artificialalso fertilizers. observed Similar in other results European were also countries observed [55 in,70 other,71]. AnacamptisEuropean countries palustris was adversely [55,70,71]. Anacamptisaffected palustris by the changeswas adversely in water affected regime by on the its changes localities—because in water regime of either on drainage or its localities—becauseexcessive of wetting either anddrainage the subsequent or excessive expansion wetting of reed.and the Thus, subsequent the remaining localities

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expansion of reed. Thus, the remaining localities need to be suitably managed in order to needsafeguard to be this suitably species. managed On the in other order hand, to safeguard E. aphyllum this and species. G. repens On theare otherforest hand,species,E. aphyllumsensitive andto changesG. repens in aresoil forest and the species, subsequent sensitive changes to changes in the in mycorrhizal soil and the subsequentcommunity changes[54,62]. Preserving in the mycorrhizal ancient forest community habitats [54 seem,62]. Preservings to be the best ancient way forest to ensure habitats the seemssurvival to beof these the best species way toin ensurethe Czech the Republic. survival of these species in the Czech Republic.

Figure 7. The highly threatened species of orchids in the Czech Republic with less than 50 sites Figure 7. The highly threatened species of orchids in the Czech Republic with less than 50 sites recorded in the last period, ranked in order of the number of occupied sites in the last period. For recorded in the last period, ranked in order of the number of occupied sites in the last period. For each species, thethe percentagepercentage survivalsurvival (orange (orange bars bars in in the the ﬁgure) figure) is is the the percentage percentage of of its its sites sites included inincluded the database in the thatdatabase have survivedthat have until survived now (wereuntil now found (were to be found occupied to be during occupied the lastduring period). the last The orchidperiod). species The orchid circled species in red circled are considered in red are to cons be theidered most to endangered be the most species endangered in the Czechspecies ﬂora in the (see textCzech for flora explanation). (see text for explanation).

4. Other Aspects That May Cause Decline in Number of Orchid Sites Of course, there are aspects other than the changes in agricultural practices that may play an important role in thethe declinedecline ofof thethe numbernumber ofof orchidorchid sites.sites. OneOne suchsuch exampleexample isis climate change. However, the effect of climate change is not thoroughly explored, and it is climate change. However, the effect of climate change is not thoroughly explored, and it out of the scope of the current manuscript. Additionally, environmental variability also is out of the scope of the current manuscript. Additionally, environmental variability also causes changes in fecundity [31]. In this paper, we found that the four most threatened causes changes in fecundity [31]. In this paper, we found that the four most threatened species are vanishing from Czech orchid ﬂora because of the excessive use or alteration of species are vanishing from Czech orchid flora because of the excessive use or alteration of their habitats, mainly caused by human impact. Thus, we emphasize protecting the natural their habitats, mainly caused by human impact. Thus, we emphasize protecting the habitats where Czech orchids occur to preserve them in their natural environment. natural habitats where Czech orchids occur to preserve them in their natural Authorenvironment. Contributions: Conceptualization, Z.Š. and P.K.; methodology, Z.Š. and P.K.; software, Z.Š. and P.K.; validation, Z.Š. and P.K.; formal analysis, Z.Š. and P.K.; investigation, Z.Š. and P.K.; resources,Author Contributions: Z.Š. and P.K.; Conceptualization, data curation, Z.Š. andZ.Š. P.K.;and writing—originalP.K.; methodology, draft Z.Š. preparation, and P.K.; software, Z.Š. and P.K.;Z.Š. and writing—review P.K.; validation, and Z.Š. editing, and Z.Š.P.K.; and formal P.K.; visualization,analysis, Z.Š. Z.Š.and andP.K.; P.K.; investigation, supervision, Z.Š. P.K.; and project P.K.; administration,resources, Z.Š. and P.K. P.K.; All authors data curation, have read Z.Š. and and agreed P.K.; writing—original to the published version draft preparation, of the manuscript. Z.Š. and P.K.; writing—review and editing, Z.Š. and P.K.; visualization, Z.Š. and P.K.; supervision, P.K.; Funding:project administration,This research receivedP.K. All noauthors external have funding. read and agreed to the published version of the manuscript. Institutional Review Board Statement: Not applicable. Funding: This research received no external funding. Informed Consent Statement: Not applicable. Institutional Review Board Statement: Not applicable. Data Availability Statement: Restrictions apply to the availability of these data. Data were obtained fromInformed the Nature Consent Conservation Statement: Not Agency applicable. of the Czech Republic and are available at https://portal. nature.cz/publik_syst/ctihtmlpage.php?what=3&nabidka=hlavni&variantaPrihlaseni=ISOP( accessed Data Availability Statement: Restrictions apply to the availability of these data. Data were on 1 February 2021) with the permission of the Nature Conservation Agency of the Czech Republic. obtained from the Nature Conservation Agency of the Czech Republic and are available at

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Acknowledgments: We thank the Nature Conservation Agency of the Czech Republic for giving us permission to use their dataset. We are greatly indebted to Tony Dixon for uncountable helpful hints as to how to improve the style of English in this paper. Conﬂicts of Interest: The authors declare no conﬂict of interest.

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